A Plant-Fungus Bioassay Supports the Classification of Quinoa (Chenopodium quinoa Willd.) as Inconsistently Mycorrhizal


Quinoa (Chenopodium quinoa Willd.) is becoming an increasingly important food crop. Understanding the microbiome of quinoa and its relationships with soil microorganisms may improve crop yield potential or nutrient use efficiency. Whether quinoa is a host or non-host of a key soil symbiont, arbuscular mycorrhizal fungi (AMF), is suddenly up for debate with recent field studies reporting root colonization and presence of arbuscules. This research seeks to add evidence to the mycorrhizal classification of quinoa as we investigated additional conditions not previously explored in quinoa that may affect root colonization. A greenhouse study used six AMF species, two AMF commercial inoculant products, and a diverse set of 10 quinoa genotypes. Results showed 0 to 3% quinoa root colonization by AMF when grown under greenhouse conditions. Across quinoa genotypes, AMF inoculant affected shoot dry weight (p = 0.066) and height (p = 0.031). Mykos Gold produced greater dry biomass than Claroideoglomus eutunicatum (27% increase), Rhizophagus clarus (26% increase), and within genotype CQ119, the control (21% increase). No treatment increased plant height compared to control, but Funneliformis mosseae increased height compared to C. eutunicatum (25% increase) and Rhizophagus intraradices (25% increase). Although quinoa plants were minimally colonized by AMF, plant growth responses fell along the mutualism-parasitism continuum. Individual AMF treatments increased leaf greenness in quinoa genotypes 49ALC and QQ87, while R. clarus decreased greenness in CQ119 compared to the control. Our research findings support the recommendation to classify quinoa as non-mycorrhizal when no companion plant is present and inconsistently mycorrhizal when conditional colonization occurs.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4


  1. 1.

    Brundrett MC (2017) Global diversity and importance of mycorrhizal and nonmycorrhizal plants. In: Tedersoo L (ed) Biogeography of mycorrhizal symbiosis. Springer International Publishing, Cham, pp 533–556

    Google Scholar 

  2. 2.

    Hirrel MC, Mehravaran H, Gerdemann JW (1978) Vesicular–arbuscular mycorrhizae in the Chenopodiaceae and Cruciferae: do they occur? Can J Bot 56:2813–2817. https://doi.org/10.1139/b78-336

    Article  Google Scholar 

  3. 3.

    Tester M, Smith SE, Smith FA (1987) The phenomenon of “nonmycorrhizal” plants. Can J Bot 65:419–431. https://doi.org/10.1139/b87-051

    Article  Google Scholar 

  4. 4.

    Cosme M, Fernández I, Van der Heijden MGA, Pieterse CMJ (2018) Non-mycorrhizal plants: the exceptions that prove the rule. Trends Plant Sci 23:577–587. https://doi.org/10.1016/j.tplants.2018.04.004

    Article  PubMed  CAS  Google Scholar 

  5. 5.

    Augé RM (2004) Arbuscular mycorrhizae and soil/plant water relations. Can J Soil Sci 84:373–381. https://doi.org/10.4141/S04-002

    Article  Google Scholar 

  6. 6.

    Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280. https://doi.org/10.1093/aob/mcp251

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  7. 7.

    Ren L, Zhang N, Wu P et al (2015) Arbuscular mycorrhizal colonization alleviates Fusarium wilt in watermelon and modulates the composition of root exudates. Plant Growth Regul 77:77–85. https://doi.org/10.1007/s10725-015-0038-x

    Article  CAS  Google Scholar 

  8. 8.

    Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant–microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739. https://doi.org/10.1093/jxb/eri205

    Article  PubMed  CAS  Google Scholar 

  9. 9.

    Brundrett MC, Tedersoo L (2018) Evolutionary history of mycorrhizal symbioses and global host plant diversity. New Phytol 220:1108–1115. https://doi.org/10.1111/nph.14976

    Article  PubMed  Google Scholar 

  10. 10.

    Wieme RA, Reganold JP, Crowder DW et al (2020) Productivity and soil quality of organic forage, quinoa, and grain cropping systems in the dryland Pacific Northwest, USA. Agric Ecosyst Environ 293:106838. https://doi.org/10.1016/j.agee.2020.106838

    Article  CAS  Google Scholar 

  11. 11.

    Vestberg M, Palojärvi A, Pitkänen T et al (2012) Neutral lipid fatty acid analysis is a sensitive marker for quantitative estimation of arbuscular mycorrhizal fungi in agricultural soil with crops of different mycotrophy. Agric Food Sci 21:12–27. https://doi.org/10.23986/afsci.4996

    Article  CAS  Google Scholar 

  12. 12.

    Urcelay C, Acho J, Joffre R (2011) Fungal root symbionts and their relationship with fine root proportion in native plants from the Bolivian Andean highlands above 3,700 m elevation. Mycorrhiza 21:323–330. https://doi.org/10.1007/s00572-010-0339-x

    Article  PubMed  Google Scholar 

  13. 13.

    Schwab SM, Johnson ELV, Menge JA (1982) Influence of simazine on formation of vesicular-arbuscular mycorrhizae in Chenopodium quinona Willd. Plant Soil 64:283–287

    Article  CAS  Google Scholar 

  14. 14.

    Azcon R, Ocampo JA (1981) Factors affecting the vesicular-arbuscular infection and mycorrhizal dependency of thirteen wheat cultivars. New Phytol 87:677–685. https://doi.org/10.1111/j.1469-8137.1981.tb01702.x

    Article  CAS  Google Scholar 

  15. 15.

    Taylor A, Pereira N, Thomas B et al (2015) Growth and nutritional responses to arbuscular mycorrhizal fungi are dependent on onion genotype and fungal species. Biol Fertil Soils 51:801–813. https://doi.org/10.1007/s00374-015-1027-y

    Article  Google Scholar 

  16. 16.

    Baon JB, Smith SE, McGraw AC (1993) Mycorrhizal responses of barley cultivars differing in P efficiency. Plant Soil 157:97–105

    Article  Google Scholar 

  17. 17.

    Hetrick BAD, Wilson GWT, Cox TS (1992) Mycorrhizal dependence of modern wheat varieties, landraces, and ancestors. Can J Bot 70:2032–2040. https://doi.org/10.1139/b92-253

    Article  Google Scholar 

  18. 18.

    Zhu Y-G, Smith SE, Barritt AR, Smith FA (2001) Phosphorus (P) efficiencies and mycorrhizal responsiveness of old and modern wheat cultivars. Plant Soil 237:249–255

    Article  CAS  Google Scholar 

  19. 19.

    Cobb AB, Wilson GWT, Goad CL et al (2016) The role of arbuscular mycorrhizal fungi in grain production and nutrition of sorghum genotypes: enhancing sustainability through plant-microbial partnership. Agric Ecosyst Environ 233:432–440. https://doi.org/10.1016/j.agee.2016.09.024

    Article  Google Scholar 

  20. 20.

    Turrini A, Giordani T, Avio L et al (2016) Large variation in mycorrhizal colonization among wild accessions, cultivars, and inbreds of sunflower (Helianthus annuus L.). Euphytica 207:331–342. https://doi.org/10.1007/s10681-015-1546-5

    Article  Google Scholar 

  21. 21.

    Murphy KM, Bazile D, Kellogg J, Rahmanian M (2016) Development of a worldwide consortium on evolutionary participatory breeding in quinoa. Front Plant Sci 7:608. https://doi.org/10.3389/fpls.2016.00608

    Article  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Kellogg J, Murphy K (2019) Evolutionary participatory Quinoa breeding for organic agro-ecosystems in the US Pacific Northwest. In: Westengen OT, Winge T (eds) Farmers and plant breeding, current approaches and perspectives. Routlege Taylor & Francis Group, Abington

    Google Scholar 

  23. 23.

    Christensen SA, Pratt DB, Pratt C et al (2007) Assessment of genetic diversity in the USDA and CIP-FAO international nursery collections of quinoa (Chenopodium quinoa Willd.) using microsatellite markers. Plant Genet Resour Charact Util 5:82–95. https://doi.org/10.1017/S1479262107672293

    Article  CAS  Google Scholar 

  24. 24.

    INVAM Factors affecting infectivity assays. In: Infect. Assays. https://invam.wvu.edu/methods/infectivity-assays. Accessed 30 Aug 2020

  25. 25.

    Yang A, Akhtar SS, Amjad M et al (2016) Growth and physiological responses of quinoa to drought and temperature stress. J Agron Crop Sci 202:445–453. https://doi.org/10.1111/jac.12167

    Article  CAS  Google Scholar 

  26. 26.

    Hinojosa L, Matanguihan JB, Murphy KM (2019) Effect of high temperature on pollen morphology, plant growth and seed yield in quinoa (Chenopodium quinoa Willd.). J Agron Crop Sci 205:33–45. https://doi.org/10.1111/jac.12302

    Article  Google Scholar 

  27. 27.

    Abbas G, Amjad M, Saqib M et al (2020) Soil sodicity is more detrimental than salinity for quinoa ( Chenopodium quinoa Willd.): a multivariate comparison of physiological, biochemical and nutritional quality attributes. J Agron Crop Sci 00:1–15. https://doi.org/10.1111/jac.12451

    Article  Google Scholar 

  28. 28.

    Vierheilig H, Coughlan AP, Wyss U, Piche Y (1998) Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl Environ Microbiol 64:4

    Article  Google Scholar 

  29. 29.

    Kormanik PP, McGraw AC (1982) Quantification of vesicular arbuscular mycorrhizae in plant roots. In: Schenck NC (ed) Methods and principles of mycorrhizal research. The American Phytopathological Society, St. Paul, pp 37–45

    Google Scholar 

  30. 30.

    McGonigle T, Miller M, Evans D et al (1990) A new method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501

    Article  Google Scholar 

  31. 31.

    R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  32. 32.

    Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67. https://doi.org/10.18637/jss.v067.i01

  33. 33.

    Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82. https://doi.org/10.18637/jss.v082.i13

  34. 34.

    Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363. https://doi.org/10.1002/bimj.200810425

    Article  PubMed  Google Scholar 

  35. 35.

    Cumming G, Finch S (2005) Inference by eye: confidence intervals and how to read pictures of data. Am Psychol 60:170–180. https://doi.org/10.1037/0003-066X.60.2.170

    Article  PubMed  Google Scholar 

  36. 36.

    Klironomos JN (2000) Host specificity and functional diversity among arbuscular mycorrhizal fungi. In: Microbial Biosystems: In: Bell CR, Brylinsky M, Johnson-Green P (eds) New Frontiers: Proceedings of the 8th International Symposium on Microbial Ecology. Atlantic Canada Society for Microbial Ecology, Halifax, Canada, pp 845–851

  37. 37.

    Treseder KK (2013) The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content. Plant Soil 371:1–13. https://doi.org/10.1007/s11104-013-1681-5

    Article  CAS  Google Scholar 

  38. 38.

    Klironomos JN (2003) Variation in plant response to native and exotic arbuscular mycorrhizal fungi. Ecology 84:2292–2301. https://doi.org/10.1890/02-0413

    Article  Google Scholar 

  39. 39.

    Smith FA, Smith SE (2013) How useful is the mutualism-parasitism continuum of arbuscular mycorrhizal functioning? Plant Soil 363:7–18. https://doi.org/10.1007/s11104-012-1583-y

    Article  CAS  Google Scholar 

  40. 40.

    Hinojosa L, González JA, Barrios-Masias FH et al (2018) Quinoa abiotic stress responses: a review. Plants 7:1–32. https://doi.org/10.3390/plants7040106

    Article  CAS  Google Scholar 

  41. 41.

    González-Teuber M, Vilo C, Bascuñán-Godoy L (2017) Molecular characterization of endophytic fungi associated with the roots of Chenopodium quinoa inhabiting the Atacama Desert, Chile. Genom Data 11:109–112. https://doi.org/10.1016/j.gdata.2016.12.015

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Pitzschke A (2016) Developmental peculiarities and seed-borne endophytes in quinoa: omnipresent, robust bacilli contribute to plant fitness. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00002

  43. 43.

    Ortuño N, Castillo J, Claros M et al (2013) Enhancing the sustainability of quinoa production and soil resilience by using bioproducts made with native microorganisms. Agronomy 3:732–746. https://doi.org/10.3390/agronomy3040732

    Article  Google Scholar 

Download references


This research would not have been possible without help from Dr. J.B. Morton, former curator of the International Culture Collection of (Vesicular) Arbuscular Mycorrhizal Fungi (INVAM) at West Virginia University. The authors thank the anonymous reviewers for critical commentary that greatly improved the manuscript.

Availability of data and material

The datasets generated during and/or analyzed in this study are available from the corresponding author upon reasonable request.

Code availability

R code is available from the corresponding author upon reasonable request.


This research was funded by Lundberg Family Farms, Richvale, California, USA, and Hatch project 1014754.

Author information




All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Julianne Kellogg. The first draft of the manuscript was written by Julianne Kellogg, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Julianne A. Kellogg.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kellogg, J.A., Reganold, J.P., Murphy, K.M. et al. A Plant-Fungus Bioassay Supports the Classification of Quinoa (Chenopodium quinoa Willd.) as Inconsistently Mycorrhizal. Microb Ecol (2021). https://doi.org/10.1007/s00248-021-01710-1

Download citation


  • Arbuscular mycorrhizal fungi
  • Quinoa
  • Bioassay
  • Host-microbe interactions